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Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes

Mario E. E. Franco Orcid Logo, Jennifer H. Wisecaver Orcid Logo, A. Elizabeth Arnold Orcid Logo, Yu‐Ming Ju Orcid Logo, Jason C. Slot Orcid Logo, Steven Ahrendt Orcid Logo, Lillian P. Moore, Katharine E. Eastman Orcid Logo, Kelsey Scott Orcid Logo, Zachary Konkel, Stephen J. Mondo, Alan Kuo, Richard D. Hayes Orcid Logo, Sajeet Haridas Orcid Logo, Bill Andreopoulos, Robert Riley, Kurt LaButti Orcid Logo, Jasmyn Pangilinan, Anna Lipzen Orcid Logo, Mojgan Amirebrahimi, Juying Yan, Catherine Adam, Keykhosrow Keymanesh, Vivian Ng Orcid Logo, Katherine Louie, Trent Northen, Elodie Drula Orcid Logo, Bernard Henrissat Orcid Logo, Huei‐Mei Hsieh Orcid Logo, Ken Youens‐Clark Orcid Logo, François Lutzoni Orcid Logo, Jolanta Miadlikowska Orcid Logo, Dan Eastwood Orcid Logo, Richard C. Hamelin, Igor V. Grigoriev, Jana M. U’Ren Orcid Logo

New Phytologist, Volume: 233, Issue: 3, Pages: 1317 - 1330

Swansea University Author: Dan Eastwood Orcid Logo

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DOI (Published version): 10.1111/nph.17873

Abstract

Although secondary metabolites are typically associated with competitive or pathogenic interactions, the high bioactivity of endophytic fungi in the Xylariales, coupled with their abundance and broad host ranges spanning all lineages of land plants and lichens, suggests that enhanced secondary metab...

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Published in: New Phytologist
ISSN: 0028-646X 1469-8137
Published: Wiley 2022
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URI: https://cronfa.swan.ac.uk/Record/cronfa59174
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Here, we examined secondary metabolite gene clusters (SMGCs) across 96 Xylariales genomes in two clades (Xylariaceae s.l. and Hypoxylaceae), including 88 newly sequenced genomes of endophytes and closely related saprotrophs and pathogens. We paired genomic data with extensive metadata on endophyte hosts and substrates, enabling us to examine genomic factors related to substrate the breadth of symbiotic interactions and ecological roles. All genomes contain hyperabundant SMGCs; however, Xylariaceae have increased numbers of gene duplications, horizontal gene transfers (HGTs) and SMGCs. Enhanced metabolic diversity of endophytes is associated with a greater diversity of hosts and increased capacity for lignocellulose decomposition. Our results suggest that, as host and substrate generalists, Xylariaceae endophytes experience greater selection to diversify SMGCs compared with more ecologically specialised Hypoxylaceae species. 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spelling 2022-10-26T13:59:50.1340593 v2 59174 2022-01-14 Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes 4982f3fa83886c0362e2bb43ce1c027f 0000-0002-7015-0739 Dan Eastwood Dan Eastwood true false 2022-01-14 SBI Although secondary metabolites are typically associated with competitive or pathogenic interactions, the high bioactivity of endophytic fungi in the Xylariales, coupled with their abundance and broad host ranges spanning all lineages of land plants and lichens, suggests that enhanced secondary metabolism might facilitate symbioses with phylogenetically diverse hosts. Here, we examined secondary metabolite gene clusters (SMGCs) across 96 Xylariales genomes in two clades (Xylariaceae s.l. and Hypoxylaceae), including 88 newly sequenced genomes of endophytes and closely related saprotrophs and pathogens. We paired genomic data with extensive metadata on endophyte hosts and substrates, enabling us to examine genomic factors related to substrate the breadth of symbiotic interactions and ecological roles. All genomes contain hyperabundant SMGCs; however, Xylariaceae have increased numbers of gene duplications, horizontal gene transfers (HGTs) and SMGCs. Enhanced metabolic diversity of endophytes is associated with a greater diversity of hosts and increased capacity for lignocellulose decomposition. Our results suggest that, as host and substrate generalists, Xylariaceae endophytes experience greater selection to diversify SMGCs compared with more ecologically specialised Hypoxylaceae species. Overall, our results provide new evidence that SMGCs may facilitate symbiosis with phylogenetically diverse hosts, highlighting the importance of microbial symbioses to drive fungal metabolic diversity. Journal Article New Phytologist 233 3 1317 1330 Wiley 0028-646X 1469-8137 Ascomycota; endophyte; plant–fungal interactions; saprotroph; specialised metabolism; symbiosis; trophic mode; Xylariales 1 2 2022 2022-02-01 10.1111/nph.17873 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University 2022-10-26T13:59:50.1340593 2022-01-14T10:46:48.6944737 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences Mario E. E. Franco 0000-0002-4959-1257 1 Jennifer H. Wisecaver 0000-0001-6843-5906 2 A. Elizabeth Arnold 0000-0002-7013-4026 3 Yu‐Ming Ju 0000-0002-8202-6145 4 Jason C. Slot 0000-0001-6731-3405 5 Steven Ahrendt 0000-0001-8492-4830 6 Lillian P. Moore 7 Katharine E. Eastman 0000-0002-4438-3854 8 Kelsey Scott 0000-0003-1378-5348 9 Zachary Konkel 10 Stephen J. Mondo 11 Alan Kuo 12 Richard D. Hayes 0000-0002-5236-7918 13 Sajeet Haridas 0000-0002-0229-0975 14 Bill Andreopoulos 15 Robert Riley 16 Kurt LaButti 0000-0002-5838-1972 17 Jasmyn Pangilinan 18 Anna Lipzen 0000-0003-2293-9329 19 Mojgan Amirebrahimi 20 Juying Yan 21 Catherine Adam 22 Keykhosrow Keymanesh 23 Vivian Ng 0000-0001-8941-6931 24 Katherine Louie 25 Trent Northen 26 Elodie Drula 0000-0002-9168-5214 27 Bernard Henrissat 0000-0002-3434-8588 28 Huei‐Mei Hsieh 0000-0002-7142-3209 29 Ken Youens‐Clark 0000-0001-9961-144x 30 François Lutzoni 0000-0003-4849-7143 31 Jolanta Miadlikowska 0000-0002-5545-2130 32 Dan Eastwood 0000-0002-7015-0739 33 Richard C. Hamelin 34 Igor V. Grigoriev 35 Jana M. U’Ren 0000-0001-7608-5029 36 59174__22299__6ca2ee634e6a4ae1896ff61f1b9a70d7.pdf 59174_AAM_and_Figures.pdf 2022-02-04T10:19:25.3763083 Output 3967638 application/pdf Accepted Manuscript true 2022-11-19T00:00:00.0000000 true eng 59174__22300__068398806eb14d979c6d1bcf82e8d8a7.pdf 59174_Supplementary_Materials.pdf 2022-02-04T10:20:52.6049463 Output 6759627 application/pdf Supplemental material true 2022-11-19T00:00:00.0000000 true eng
title Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
spellingShingle Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
Dan Eastwood
title_short Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
title_full Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
title_fullStr Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
title_full_unstemmed Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
title_sort Ecological generalism drives hyperdiversity of secondary metabolite gene clusters in xylarialean endophytes
author_id_str_mv 4982f3fa83886c0362e2bb43ce1c027f
author_id_fullname_str_mv 4982f3fa83886c0362e2bb43ce1c027f_***_Dan Eastwood
author Dan Eastwood
author2 Mario E. E. Franco
Jennifer H. Wisecaver
A. Elizabeth Arnold
Yu‐Ming Ju
Jason C. Slot
Steven Ahrendt
Lillian P. Moore
Katharine E. Eastman
Kelsey Scott
Zachary Konkel
Stephen J. Mondo
Alan Kuo
Richard D. Hayes
Sajeet Haridas
Bill Andreopoulos
Robert Riley
Kurt LaButti
Jasmyn Pangilinan
Anna Lipzen
Mojgan Amirebrahimi
Juying Yan
Catherine Adam
Keykhosrow Keymanesh
Vivian Ng
Katherine Louie
Trent Northen
Elodie Drula
Bernard Henrissat
Huei‐Mei Hsieh
Ken Youens‐Clark
François Lutzoni
Jolanta Miadlikowska
Dan Eastwood
Richard C. Hamelin
Igor V. Grigoriev
Jana M. U’Ren
format Journal article
container_title New Phytologist
container_volume 233
container_issue 3
container_start_page 1317
publishDate 2022
institution Swansea University
issn 0028-646X
1469-8137
doi_str_mv 10.1111/nph.17873
publisher Wiley
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
document_store_str 1
active_str 0
description Although secondary metabolites are typically associated with competitive or pathogenic interactions, the high bioactivity of endophytic fungi in the Xylariales, coupled with their abundance and broad host ranges spanning all lineages of land plants and lichens, suggests that enhanced secondary metabolism might facilitate symbioses with phylogenetically diverse hosts. Here, we examined secondary metabolite gene clusters (SMGCs) across 96 Xylariales genomes in two clades (Xylariaceae s.l. and Hypoxylaceae), including 88 newly sequenced genomes of endophytes and closely related saprotrophs and pathogens. We paired genomic data with extensive metadata on endophyte hosts and substrates, enabling us to examine genomic factors related to substrate the breadth of symbiotic interactions and ecological roles. All genomes contain hyperabundant SMGCs; however, Xylariaceae have increased numbers of gene duplications, horizontal gene transfers (HGTs) and SMGCs. Enhanced metabolic diversity of endophytes is associated with a greater diversity of hosts and increased capacity for lignocellulose decomposition. Our results suggest that, as host and substrate generalists, Xylariaceae endophytes experience greater selection to diversify SMGCs compared with more ecologically specialised Hypoxylaceae species. Overall, our results provide new evidence that SMGCs may facilitate symbiosis with phylogenetically diverse hosts, highlighting the importance of microbial symbioses to drive fungal metabolic diversity.
published_date 2022-02-01T04:16:16Z
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